Abstract

Background

In insect classical conditioning, octopamine (the invertebrate counterpart of noradrenaline)
or dopamine has been suggested to mediate reinforcing properties of appetitive or
aversive unconditioned stimulus, respectively. However, the roles of octopaminergic
and dopaminergic neurons in memory recall have remained unclear.

Results

We studied the roles of octopaminergic and dopaminergic neurons in appetitive and
aversive memory recall in olfactory and visual conditioning in crickets. We found
that pharmacological blockade of octopamine and dopamine receptors impaired aversive
memory recall and appetitive memory recall, respectively, thereby suggesting that
activation of octopaminergic and dopaminergic neurons and the resulting release of
octopamine and dopamine are needed for appetitive and aversive memory recall, respectively.
On the basis of this finding, we propose a new model in which it is assumed that two
types of synaptic connections are formed by conditioning and are activated during
memory recall, one type being connections from neurons representing conditioned stimulus
to neurons inducing conditioned response and the other being connections from neurons
representing conditioned stimulus to octopaminergic or dopaminergic neurons representing
appetitive or aversive unconditioned stimulus, respectively. The former is called
'stimulus-response connection' and the latter is called 'stimulus-stimulus connection'
by theorists studying classical conditioning in higher vertebrates. Our model predicts
that pharmacological blockade of octopamine or dopamine receptors during the first
stage of second-order conditioning does not impair second-order conditioning, because
it impairs the formation of the stimulus-response connection but not the stimulus-stimulus
connection. The results of our study with a cross-modal second-order conditioning
were in full accordance with this prediction.

Conclusion

We suggest that insect classical conditioning involves the formation of two kinds
of memory traces, which match to stimulus-stimulus connection and stimulus-response
connection. This is the first study to suggest that classical conditioning in insects
involves, as does classical conditioning in higher vertebrates, the formation of stimulus-stimulus
connection and its activation for memory recall, which are often called cognitive
processes.